Evolutionary ecology of brains

Question 1

Why do we look at brain size?

Answer 1

Easily measured
Can be predicted by fossil record, although some taxa have a poor fossil record e.g. primates (best to model using Bayesian analysis)
Provides an estimate of some other neural parameter/s responsible for intelligence

Question 2

Brain and body and constraints

Answer 2

Brain size scales with body size - Jerison thought it was constrained by SA:V ratio of body, Martin thought basal metabolic rate
Brain growth and body growth have different ontogenic trajectories - e.g. in mammals, brain growth ceases long before body growth.
Brain/body allometry is specific to each taxon
Balaban et al 1988 - Inter-specific transplantation experiments in birds showed body size does not dictate brain size.
Metabolic cost of brain in vertebrates is 2-10% of total. 20% in humans, despite being 2% of body mass
BMR relative to body mass increases with relative brain size

Question 3

Evidence selection can act on total brain size - experimental

Answer 3

We can artificially select for big or small brains in mice and guppies
Kotrschal et al - developed guppy lines that differed in relative brain size by 9%. Found large-brains improved numerical learning ability in females, and spatial learning ability in males. Later found large brains conferred a more proactive personality. But small-brained animals had lower gut mass and fewer offspring.

Question 4

Evidence selection can act on total brain size - phylogenetic analyses

Answer 4

Looking at primate phylogeny, a model biased towards directional selection fit brain size evolution best, while a model of random direction of change fit body mass evolution best.
Montgomery et al 2010 - systematically analysed primate ancestral phylogeny. whilst brain size decreases along some phylogenetic lines, overall absolute and relative brain size increases, whilst body size does not. The human lineage is interesting only in absolute brain mass increase.

Question 5

Evidence selection can act on total brain size - molecular

Answer 5

Large-brains in guppies was associated with increased expression of Ang-1, which controls neurogenetic activity of neural progenitor cells
Human specific changes in FoxP2 have increased synaptic plasticity in circuits surrounding language and speech
In microcephaly, asymmetric division of neural progenitors begins too early. Caused by mutations in ASPM (which interacts with CITK to organise and orient the astral microtubules). ASPM coevolved with brain mass but not body mass
(remember selection–>genes–>brain size

Question 6

Evidence that overall brain size relates to cognition

Answer 6

Innovation = spontaneous production of a new behaviour in response to environmental stimulus. Innovation correlates with relative brain size in primates and birds
Absolute brain mass correlated with ‘global cognition’ in primates, as measured by 9 tests
Absolute brain mass correlates with success in self-control tests
Relative brain size and absolute brain mass correlated with problem-solving tests
Kotrschal et al’s bigger brained guppies were better at numerical (female) and spatial (male) tests

Question 7

Problems with evidence linking overall brain size to cognition

Answer 7

Behavioural tests assume trial+error or associative learning as equivalent to understanding - Logan 2016 found no correlation in individual performance in innovation and reversal learning tasks.
Global cognition appears to explain less than 40% of variation. Correlation between g and brain size in humans is very weak (r=0.2-0.3)
Why should animals pay attention to humans trying to train them? Why do we judge intelligence by human standards/tests? Must take into account ecological differences between taxa when measuring ‘intelligence’
Brain size may not matter (think neuronal density, cellular characteristics, genetics)

Question 8

For concerted evolution

Answer 8

Concerted brain hypothesis - allometry between regions is due to order of neurogenesis, e.g. neocortex develops later and hence is disproportionately bigger as overall brain size increases. Developmental conservatism constrains brain structure.

Brain scaling is conserved across taxa, and order of neurogenesis is conserved between mouse and monkey (this suggests strong developmental constraints, and component size determined by brain size. Selection acts through brain size)

Question 9

For mosaic evolution

Answer 9

There are grade shifts in relative neocortex size between taxa (grade shifts mean altered y-intercept, which in a brain size-body size graph will be log(allometric constant), constant thought to be the encephalisation quotient (Jerison). When effects of grade shifts are taken into account, neocortex scales nearly isometrically

Partial correlations among individual components vary between groups, matching functional connectivity

Functional coevolution pervades biological levels, and is apparent in volume of components, volume of subcomponents, and cellular composition (neuron density varies across brain regions, so increasing mass of different regions will increase overall brain size to different extents)

Interspecific variation in component size (e.g. primates have higher neuron densities in the cerebellum and neocortex than other mammals) is more strongly correlated with ecology than overall brain size

Patterns of covariance between components can themselves be selected on.

(suggests strong functional constraints, and component size determined independently of brain size. Selection acts on individual brain components)

Question 10

Evidence against size mattering

Answer 10

When human FoxP2 was put in mice, they had improved performance in learning tasks and altered development of basal ganglia, but NOT bigger in any region of the brain.
Han et al 2013 - Grafting human glial progenitor cells into neonatal mice led to improved LTP and improved learning. so why should we focus on neuron density/number?!
Can’t ignore cellular composition/properties - elasmobranchs have much bigger brains than teleosts but much lower energy consumption because less Na/K pump.
Neuron number and volumetric proportions are uncorrelated
It is circular to argue that size, or executive brain ratio, or neocortex size is a good measure of cognition simply because that measure supports your hypothesis.

Question 11

Expensive brain/tissue hypothesis

Answer 11

Expensive brain hypothesis - across primates, relative gut size is inversely correlated with relative brain size
Kotrschalz’s large-brained guppies had smaller guts
Expensive tissue hypothesis - the actual tradeoff is with adipose deposits
When fat is included separately in the analysis, the gut increases in size with the brain.
Investment in fat and big brains may be redundant safeguards against unpredictable food supply

Question 12

Constraints lifted by big brains

Answer 12

Mammals with bigger brains live longer - perhaps longer memory needed and behavioural flexibility because they’ll experience more changes? Does brain size limit lifespan, or does lifespan limit brain size? Latter possible, but in mammals brain stops growing in adolescence.
Requirement for large fat stores
…requirement for many offspring?

Question 13

Adjustments required to support big brains

Answer 13

Longer gestation and increased maternal energy turnover to support neurogenesis
Increased lactation duration to support synaptogenesis, axon and glial growth
Birds with large relative brain size have longer incubation periods, later fledgling ages, longer post-fledling care. More altricial development may require more biparental care, which is supported by increased pair bonding.
–Gonzales-Voyer et al 2009 - female but not male brain size in cichlids was increased with uniparental care, i.e. the cognitive load was on the mother. –
Migratory distance decreases as relative brain size increases across bird species
Increased relative brain size in carnivores is associated with diet quality (e.g. insectivores have smaller brains than carnivores)
Relative brain size in primates correlates with frugivory - fruits are more calorific and easier to digest. BUT frugivores also have wider home ranges, is the correlation just because bigger brain + spatial memory allows frugivory? No, because hippocampus size does not correlate with home range, and brain size does not correlate with home range size when controlling for frugivory.
Increased food processing - apes preferentially eat cooked meat when given the choice, and mice grow better if you feed them cooked food. But this one’s hard to tell if it’s allowing or requiring a big brain…

Question 14

Specific examples supporting mosaic evolution

Answer 14

Cave fish have smaller optic tectum than surface-dwelling fish, but not smaller brain overall.
In sticklebacks, heritability of relative size of brain regions was low, and genetic correlation was low. having low genetic covariance reduces likelihood that evolution of one region will be constrained by change in a correlated region reducing fitness.
Primates had high heritability in brain structures only after correcting for total brain size (i.e. so variation is not by some overall total brain size gene)

Question 15

Potential genetic mechanisms of mosaic evolution

Answer 15

Genes might:
shift boundaries in progenitor pool prior to neurogenesis (to alter relative sizes but not overall size. Demonstrated in African cyclids; morphogen patterning along rostro-caudal axis increases telencephalon)
region-specific increased duration of neurogenesis (telencephalic neurogenesis is delayed in passerine birds, which increases number of cells destined for telencephalon)
region specific increased rate of neurogenesis (Period of accelerated cell cycling occurs in galliform birds. Differences in genes linked to human brain expansion have been shown to alter cell cycling)

Question 16

Brain expansion and sensory adaptation

Answer 16

Brain regions responsible for the same sensory modality co-evolve, those for different modalities do not.

Sensory specialisation in brain structure (as seen in cave fish) is due to ecology, not a trade-off - frugivory in nocturnal primates expands olfactory cortex, in diural primates expands visual cortex, but in bats expands both. Bats show it’s not a biological constraint, there’s just not a selection pressure to have both in the primates.

Degree of binocularity in primates correlates with total brain size, and with relative number of parvocellular neurons in LGN. Relative size of cortical and subcortical visual structures correlates with overall neocortex size and relative brain size. So maybe visual evolution accounts for expansion?
In humans, V1 is reduced relative to rest of neocortex, but parietal areas in dorsal stream (magnocellular) expanded compared with macaques. So primates have evolved for detail, we’ve evolved away from this towards movement?

Relative visual cortex size in primates correlated with relative facial nucleus size, which also correlated with grouo size. Links sensory theory to social theory?

Question 17

Social brain hypothesis - evidence linking big brains to social behaviour

Answer 17

Dunbar and Schultz, 2007 - relative neocortex size correlates with group size in primates, esp with female cohort size
relative neocortex size is higher in pair-bonded bird species
Maybe the primate effect is because friendships are basically platonic pair-bondings?
Individual differences in group size correlate with volume differences in frontal and temporal regions in humans and macaques
Primates with larger brains have higher rates of social learning
Primates with a larger neocortex show more tactical deception
Kotrschalz et al - big brained guppies exhibited more proactive behaviour

Question 18

Machiavellian Intelligence Hypothesis

Answer 18

Groups are intrinsically competitive and exploitative.
But e.g. herd of cows aren’t
If groups are so exploitative, why stay in them? SO MIH is effect, not cause, of social group size

Question 19

Social brain hypothesis - why live in groups?

Answer 19

Living in big groups can’t be dismissed as a byproduct of big brains because it is so costly to live in a big group - competition, stress, time sink.
female baboon longevit and fecundity correlate with number of social partners, so social groups improve fitness, so the bigger brain required is worth the cost.

Question 20

Social brain hypothesis - mechanism behind it

Answer 20

A problem is solved socially
A big brain is required to achieve the requisite sociality
It’s the complexity of these relationships that is important. Sociality is ‘building and maintaining complex social relationships’. Simple group size correlation is only found in primates… perhaps because their interactions are by default complex?

Question 21

Brain expansion and foraging style

Answer 21

Relative brain size in primates correlated with frugivory, and not with home range when controlling for frugivory.
Frugivory correlates with neocortex size when controlling for home range size.
No association between hippocampus and home range size

Controlling for group size erased the frugivory-brain size correlation. So perhaps big groups need big brains which need frugivory

Extractive foraging (using tools) correlated with executive brain ratio in primates.
BUT innovative foraging is either abundant in a species or not there at all, so cannot account for continuous variation in brain size

Neocortex and cerebellum coevolve, and both correlate with relative brain size. One exception is the cerebellar expansion seen in primates and other extractive foragers. Both are likely to contribute to both social and physical intelligence.

Question 22

Summary of ecological pressures on brain size

Answer 22

Activity patterns (diurnal vs nocturnal)
Diet
Group size
Method of foraging (innovative/extractive)
Stereoscopic convergence

It’s likely all of these selective pressures cause complex patterns of coevolution in independent brain structures, patterns which vary between species. Remember selection acts on the behaviour/system, not on any neuroanatomical parameter.

Question 23

Genetic explanations for primate brain evolution

Answer 23

I.e. we have a gene mutation that allows big brains.
For - FOXP2, Ang-1
Against - low genetic correlation between different brain regions

Question 24

Developmental explanations for primate brain evolution

Answer 24

More parental investment allows bigger brains

For - birds that exhibit biparental care have bigger brains. Humans have longer post-natal dependence on parents, longer gestation, longer duration of lactation. For females, more parental investment means a bigger brain (i.e. bigger female brains in uniparental cichlids).

Against - In humans, the maternal brain shrinks by up to 7% during gestation (Oatridge et al 2002). Extensive biparental care is seen in a wide variety of small-brained animals. Brain size is negatively correlated with fecundity (guppies). Ebneter et al 2016 found that increased prenatal maternal investment in the Japanese quail negatively correlated with cerebellum size, so parental investment could limit brain size, or vice versa. But others found that birds with larger brains have longer incubation time, older fledgling age, so maybe the quail thing was because they were artificially selected?

Question 25

Ecological explanations for primate brain evolution

Answer 25

Foraging better, living in bigger groups etc required bigger brains to develop.

Against - but why should animals need to do those things? Probably to support a bigger brain! So not a cause of brain development, but a solution to a constraint

Question 26

Cultural Intelligence Hypothesis

Answer 26

Apes are social, but humans are ‘ultra-social’, able to produce shared fictions and theory of mind. This allows development of cultures

For - Hermann et al 2007 - while chimps and 2.5 y/o children had similar cognitive skills to deal with the physical world, the children were better at dealing with the social world. In primates neocortex volume is best predicted by length of socialisation period (weaning–>1st reproduction), not parental investment period, so learning. Learning supposedly allows smart foraging.

Against - Altmann showed foraging skills are learnt before weaning, so can’t be the result of cultural exposure. Populations of apes show group-specific traditions/behaviours, which can be transmitted socially. I.e. they have culture.

Question 27

Insect brains can do complex stuff

Answer 27

Bees can solve a string pulling test
Bees can learn from others
Wasps recognise faces
Bees can count to four
Ants count their footsteps (lengthened or shortened their legs, and they overshot their nests in a predictable manner)

Question 28

Anatomy of an insect brain

Answer 28

Each component is called a neuropil, regions of the brain with high density of synapses
Visual processing is in the optic lobes in nested structures: lamina (which receive directly from the compound eye) then medulla, then lobula. Labelled line for light, colour, motion. Potential specialisation of functional classes of neurons
Olfactory processing is input from receptor cells in antennae, onto glomeruli (mostly receptor-specific, note convergent evolution and olfactory map) in antennal lobes, interneurons connect glomeruli to create ‘combinatorial code’, then relayed to mushroom bodies and lateral horn
These sensory neuropils project to the rest of the brain for integration with interoceptive and memory information.
Central complex is a multi-functional sensorimotor integration centre linked to orientation, navigation and locomotor control
Mushroom bodies, formed of Kenyon cells (dendrites form the calyx, axons form the pedunculus and lobes), linked to learning

Question 29

Insect olfactory system - variation depending on ecology

Answer 29

Nocturnal lepidoptera (moths) have larger antennal lobes, due to increase in glomeruli number, not volume.
But even the diurnal ones have larger AL than butterflies, due to macroglomeruli (adaptations to detect e.g. long-range pheromones).
There are male-specific macroglomeruli in moths, and caste-specific in leaf cutter ants (because they use them to follow the trail). Does this mean caste is genetically encoded? Or is glomerulus size phenotypically plastic?
D. sechellia oviposits on morinda fruit, whose volatiles are dominated by acids. DS has more acid sensing sensilla than D melanogaster, and duplicated and expanded acid glomeruli --> macroglomeruli. So selection modified both peripheral and AL structure

Question 30

Insect visual system - variation depending on ecology

Answer 30

In Heliconius, duplication of UV-sensitive opsin coincides with evolution of a UV reflectant yellow pigment, used for intra-specific communication (birds can’t see it)
Most diurnal species - apposition eyes, where photoreceptors receive light from single ommatidium lens–> high spatial resolution
Most nocturnal species - superposition eyes, where photoreceptors and lenses separated by a clear zone, so multiple photoreceptors sample each lens –>high sensitivity

Secondarily nocturnal - Megalopta genalis, has an apposition eye but with big facets.

In crepuscular lepidoptera, lamina monopolar cells (which process inputs from photoreceptors) have more lateral branching dendrites, thus increased connections between lamina cartridges, and perhaps spatial summation

Diurnal lepidoptera have bigger visual neuropil and smaller ALs, and having learnt stimulus-reward associations for both visual and olfactory stimuli, will choose the visual cue when both are presented! This is not a difference in perception, just in weighting.

Whirligig beetles have two sets of eyes, and split visual neuropil, specialised for air and water vision.

Question 31

Mushroom body functions, adaptation

Answer 31

Ablate KCs in Drosophila during window when they’re the only proliferating cells, using hydroxyurea. They can’t form olfactory memories (so can’t be conditioned).

vertical (alpha) lobe of mushroom body KO impairs long term memory

Physical MB ablation in cockroaches impairs spatial learning

Whirligig beetles are anosmic - AL have no glomeruli, are only for mechanoreception. Visual input has taken over MB circuitry from olfactory input.

Hawkmoth MB is multi-modal. Size of area dedicated to visual/olfactory input corresponds to activity pattern.

MBs are highly plastic, with age dependent and experience dependent effects in Hymenoptera

Question 32

Mushroom body expansion, focus on foraging

Answer 32

There’s been convergent evolutionary expansion of the MB, so it can be up to 40% of neurons, where in Drosophila it’s 4-5%.
In scarab beetles, generalists (herbivore and insectivore) have double calyx, more KCs, higher synaptic density, gyrenfication (folding). Specialists receive sensory input from fewer environments, so single calyx and lower neuron density.
Hymenoptera (ants and bees) both have MB expansion. First thought this was because they’re both social, but now allocentric foraging
-MB expansion occured with origin of parasitoidism, and 90myr before evolution of social species.
-Foraging experience associated with increased dendritic branching of KC, increased number but sometimes decreased density of synapses, increased total MB volume, and especially in collar.
In Heliconia, wild-caught animals have bigger MBs, and old lab-reared have slightly bigger than young. Suggestion is that having to forage has increased it, but maybe the better diet facilitated it? Experience-dependence is just opportunistic?

Question 33

Summary of visual adaptations in insects

Answer 33

Duplication of receptors (heliconia UV)
Alteration in accessory structures (apposition vs superposition eyes)
Altered cellular morphology (more LMC dendritic branching)
Size of neuropil

Question 34

Summary of olfactory adaptations in insects

Answer 34

Peripheral receptor changes (more acid sensing sensilla  in D sechellia)
Processor changes (more acid-associated glomeruli)
Macroglomeruli (for sex pheromones, or trail following)
Volumetric changes in AL (moths vs butterflies, nocturnal vs diurnal)

Question 35

Comparing small insect brains to big animal brains

Answer 35

Insects can count, can pay attention, and can categorise visual stimuli (symmetric vs asymmetric). Contextual learning, sequence learning, social learningNeural network analyses show these skills require v few neurons.
Simply making brains bigger should just give us more of the same (quantitative not qualitative change).
Larger brains have more repetition of neural circuits, which adds precision, but is unlikely to underlie the qualitative shift in behaviour that assumed from insects to animals
Instead, interconnectivity and modularity may be important.